BACKGROUND:
development assessment of preterm infants. AIM: to evaluate the association between the gestational ages (GA) of
premature infants with the global motor development as well as with early signs
of sensory oral motor development delay, and to verify a possible association
between them.METHOD: an exploratory study that assessed the development of 55 infants
with corrected chronological ages between four to five months, born preterm
at the Instituto Materno Infantil Professor Fernando Figueira (IMIP) and who
were followed at the Kangaroo Mother Program Clinic between March and August
of 2004. The assessment of the sensory oral motor development was performed
through pre-selected indicators and of the global motor development through
the Alberta Infant Motor Scale (AIMS).RESULTS: infants with lower GA (29 to 34 weeks) presented a higher median
of risk signs in the sensory oral motor development assessment when compared
to those with higher GA (35 to 36 weeks). Regarding the global motor development,
infants born with lower GA presented a higher number of scores in the AIMS below
percentile 10 (26%) when compared to those with a higher GA (4%) (p=0.009).
The median index of the risk signs for the sensory oral motor development were
significantly higher among infants with total AIMS scores below percentile 25
when compared to those with scores equal to or above percentile 25.CONCLUSION: the gestational age of infants at birth influenced the sensory
oral motor and global motor development - infants with lower gestational ages
presented worse performances. These findings suggest a possible association
between both aspects of infant development.

The advances in perinatal and neonatal care have led to
increased survival among newborns with ever-lower gestational age
and birth weight. However, these babies require careful
follow-up, since they present greater vulnerability with regard
to abnormalities of neuropsychomotor development (Aurélio
et al., 2002; Mancini et al., 2002).

It is observed that, at birth, premature infants have
abilities that correspond to their state of maturity. Their
exposure to neonatal intensive care and an interactional history
that is greatly brought forward require competencies that do not
exist yet, thus overloading their process of full development.
Therefore, professionals who follow up the evolution of these
babies must be alert towards detecting abnormalities and
undertaking early intervention. Assessment of overall motor
development and oral sensorimotor development is an important
part of this follow-up (Méio et al., 2004; Rugolo, 2005)
.

The theory of dynamics systems proposes that movement and
changes in their patterns are generated by various systems in
which the components interact and become organized. Within this
context, many authors have emphasized that comprehensive
assessment of orofacial motricity not only includes observation
of oral motor control and sensory responses but also includes
other factors such as body weight, muscle strength, weight
support, attention, specific context of the environment and the
complexity of the task offered (Piper and Darrah, 1994; Morris
and Klein, 2000; Howle, 2002; Monson et al., 2003; Rocha et al.,
2005; Rogers and Arvedson, 2005).

Although most preterm newborns do not develop severe
neurological abnormalities like cerebral palsy, mental deficiency
or epilepsy, so-called minor developmental disorders are very
prevalent in this population. Prominent among these are attention
deficit, minor overall and oral motor abnormalities, delayed
language development and behavioral disorders. It has been shown
that minor deficits become more visible with increasing age,
especially from the fifth month of life onwards. These signs are
often not identified at an early stage, because of the lack of
measurements that are sufficiently sensitive for detecting motor
and behavioral problems within this age group (Wolf et al., 2002;
Fontenele et al., 2004; Rugolo, 2005).

Because of this,
the present study had the objectives of evaluating associations between the
gestational age of infants born prematurely and their overall motor development
and between the gestational age and early signs of abnormalities in oral sensorimotor
development, and of investigating the possibility of an association between
overall and oral sensorimotor development.

Method

Ethical approval

The present study was approved by the Ethics Committee for
Research on Human Beings of the "Professor Fernando Figueira"
Mother and Child Institute, under protocol number 264. Free and
informed consent in writing was obtained from the persons
responsible for the infants that were included in the study, and
all the subjects involved gave their consent for the study to be
carried out and for its results to be published.

Study population and location

The present research consisted of an exploratory study that
was carried out at the outpatient department of the Kangaroo
Mother Program of the "Professor Fernando Figueira" Mother and
Child Institute (IMIP). The interdisciplinary team of this
institute consists of pediatricians, nurses, speech therapists,
occupational therapists, physiotherapists and psychologists.
These professionals systematically follow up the growth and
development of infants who were at risk, from birth to two years
of life.

Fifty-five preterm infants were included in the present study.
Preterm birth was defined as a gestational age of less than 37
weeks, as assessed by a neonatologist during the first 24 hours
of life by means of the Capurro method (Capurro et al., 1978).
They were assessed when they were four to five months old
(chronological age corrected to a gestational age of 40 weeks),
at a routine outpatient consultation between March and August
2004. The exclusion criteria for the study were multiple
pregnancy, neurological abnormalities during the neonatal period,
genetic syndromes and congenital malformations.

Sociodemographic, feeding and biological characteristics of
the children

The infants' mothers or caregivers were questioned regarding
socioeconomic and demographic conditions, current feeding
practice and signs of abnormality regarding extra-oral and
intra-oral tactile sensitivity. Information on birth weight,
gestational age, morbidity and procedures carried out during
hospital stay were obtained through analysis of the medical
records.

The breastfeeding definitions used were the ones adopted by
the World Health Organization, and thus exclusive breastfeeding
was considered to be maternal milk intake without any supplements
(water, other liquids or solids) during the whole day. Partial
breastfeeding was considered to be when the infant took breast
milk with other supplements (water, juice, tea, artificial milk
or solids) (WHO, 1992).

Assessment of oral sensorimotor development

This assessment was conducted by two authors (the speech
therapists ACG and RRA). To test the research forms and
standardize the assessment technique, a pilot study involving 10
infants was carried out.

The oral sensorimotor development was assessed by means of a
protocol drawn up by the principal investigator (ACG) that was
based on the evolution of normal development among infants from
four to five months of age, in accordance with the Bobath
neuroevolution concept and the Alexander, Boheme and Cupps
assessment (1993). When the observed developmental item was what
was expected (normal), it was coded as zero (0), and when it was
not what was expected (sign of risk), it was coded as one (1).
The sum of the signs of risk resulted in an assessment index for
the oral sensorimotor system that could range from 0 to 15.

The infants were examined in the prone and supine postures on
a standard mat and when seated on the examiner's lap.
Manipulations were performed, consisting of touching the face and
oral cavity (proprioceptive tactile stimulus), sometimes with the
examiner's hands and sometimes with a standardized toy made of
very flexible rubber.

In this group, the infants were monitored for the presence of
rooting, suckling, gagging and phasic bite reflexes. At the age
studied, the presence of any of these reflexes was considered to
be a risk factor.

The rooting reflex was assessed by means of touching the
cheeks and perioral region and was considered to be present when
the infant turned its head and opened its mouth in the direction
of the stimulus.

The suckling reflex was assessed by introducing a gloved
finger into the infant's oral cavity, between the tongue and the
hard palate, and observing whether grasping occurred and rhythmic
suction started.

The gagging reflex was tested by touching the gloved index
finger on the anterior medial and posterior regions of the tongue
and following towards the uvula, posterior wall of the pharynx
and soft palate. The reflex was present when, at the time the
mouth was open, the head was pulled back and the infant
scowled.

The phasic bite reflex was assessed by stimulating the lateral
region of the lower gums, and it was considered present when the
infant made sequenced chewing movements without contracting the
buccinator muscles on the side of the stimulus, as seen by the
contraction of the cheek on this side.

Oral motor structures

This group was assessed by observing the oral structures
(lips, tongue, cheeks, mandible and larynx) in activity and at
rest, while the infant was exploring a very flexible rubber toy.
Absence of the activities or postures described in the following
was considered to be a risk factor at this age:

To assess the lips, the infant's activity on the mat in the
prone position was observed. The expected posture was that the
infant would support its weight on its forearms, with contraction
and stretching of the upper lip and lip closure.

To assess the tongue, the infant's position was not
standardized. When the rubber toy was introduced into the
infant's oral cavity, the examiners assessed the activity of the
tongue in the frontal movement plane, as observed by the presence
of contraction of the tongue in the lateral region.

The activity of the cheeks was investigated according to
symmetrical contraction of the buccinator muscles, unilateral
contraction and symmetrical smile. With the infant on the
examiner's lap, a rubber toy was introduced into the oral cavity
above the tongue. This maneuver was expected to trigger
symmetrical contraction of the buccinator muscle. To assess the
lateral contraction of this muscle, the toy was positioned
laterally in the oral cavity, with an expected response of
contraction of the buccinator muscle on the side of the stimulus.
The presence of a symmetrical smile was assessed during
interaction with the examiner, mother and/or caregiver.

Synergic contraction of the levator and depressor muscles was
observed for assessing the activity of the mandible, with the
infant on the investigator's lap, while exploring the intra-oral
region with the toy. The mandible was expected to be aligned with
the maxilla, with sufficient excursion of its condyles to enable
opening and closing.

The posture of the larynx was assessed with the infant in the
prone position on the mat. For the laryngeal posture to be
considered adequate (start of its descent), the investigator
observed that when looking at the toy that was on the mat, the
infant kept its neck stretched and supported the weight of its
upper trunk on its forearms.

The presence of normal laryngeal elevation movement during
deglutition was assessed with the infant on the investigator's
lap, exploring the rubber toy in the oral cavity, thereby
stimulating the production of saliva that was then swallowed.

Oral emissions

The levels of oral emissions were assessed by means of
interaction between the infant and the examiner, with toys,
and/or with the infant's mother/caregiver. Absence of guttural
sounds (gargles) and vocalization during the assessment was
considered to be a risk factor.

Symmetrical activity of the arms

With the infant seated on the examiner's lap or in the supine
position on the mat, it was observed whether the infant had the
capacity to bring the toy to its mouth with the arms acting
symmetrically. Absence of this activity was considered to be a
risk factor.

Assessment of overall motor development

Overall motor development was assessed by using the Alberta
Infant Motor Scale (AIMS), which consists of a test that observes
the quality of the movement components, such as the infant's
ability to transfer its weight, posture adopted in motor tasks
and control over muscles that work against gravity. The scale is
composed of 58 items divided into four subscales: 21 items in the
prone posture; 9 in the supine posture; 12 in the seated posture
and 16 in a standing posture. This scale is applicable from birth
to 18 months of age.

The result from
the assessment consisted of a dichotomized choice for each item, which had to
be assessed as "observed" or "not observed". Each item observed in the infant's
motor skill repertoire received a score of one, and each item not observed received
a score of zero. The observed items on each of the subscales were summed, thus
resulting in four subtotals for the subscales of prone, supine, seated and standing.
The total score for the test was given by the sum of the subtotals, and could
be converted into a motor performance percentage that was established on the
basis of the normative sample for the test (Piper and Darrah, 1994).

Results

The statistical treatment for the data was done using the
statistical package Epi-Info version 6.04 (CDC, Atlanta). The
typing of the data was done with double data entry, thus enabling
its validation. Since the oral sensorimotor development index
presented asymmetric distribution, the median and quartiles were
used as central trend and dispersion measurements, respectively.
The tests for statistical significance used were the chi-squared
test for the categorical variables and the non-parametric
Kruskal-Wallis test for continuous variables. The significance
level adopted was p 0.05.

Table
1 shows that 75% of the families were classified as poor, with per capita
income of less than half a minimum monthly salary. Around 26% of the mothers
were adolescent, 82% of them were primiparae, all had been to school and 60%
had reached high school level, with or without completing it.

Among the infants studied, in the neonatal phase 56% had a
gestational age of less than or equal to 34 weeks, with a minimum
of 29 weeks. All the newborns (except two) presented birth weight
of less than 2000g, and 37% of them had birth weight of less than
1500g (the highest birth weight was 2690g). Most of the newborns
(87%) presented an Apgar score of eight of more at the fifth
minute of life. Among the most frequent neonatal morbidities were
respiratory adaptation syndrome (59%), respiratory discomfort
syndrome (19%) and hyperbilirubinemia (68%). It was observed that
67% of the newborns remained in hospital for 30 days or less, and
76% of them were in the rooming-in of the Kangaroo Mother Program
for 15 days or less. The maximum duration of gavage diet was 58
days, while 41% of the newborns required feeding by intubation
for between two and three weeks. The transition from gavage diet
to oral feeding took an average of nine days and did not exceed
17 days. Translactation was performed for 67% of the newborns and
78% of the sample was followed up by a speech therapist during
the hospital stay.

At the time of the assessment, 23 infants (42%) had a
chronological age of five months, 25 (45%) of six months and 7
(13%) of seven months, which corresponded to 38 infants (69%)
with a corrected age of four months and 17 (31%) of five
months.

Table
2 shows that 78% of the infants were not receiving exclusive breastfeeding
at the time of the assessment and 44% were using pacifier. Only 5% of the infants
demonstrated dissatisfaction at the time of feeding, 9% did not like being caressed
on the face, 29% demonstrated discomfort when their faces were being cleaned
and also 67% rejected stimuli with a rough texture on the face. Among the infants
who were not exclusively breastfed, 63% of the mothers used their hand to introduce
food into the oral cavity of their children and for 84% of the infants the food
was offered on a spoon. Among the 43 infants who were being bottle-fed, 16%
rejected it and 70% of the mothers had increased the hole in the teat to obtain
a greater flow of the diet. Of the 36 infants who were being fed using a spoon,
mashed fruits and vegetables were more frequently offered, although the mothers
said that 25% of the infants did not like this diet. The time spent on feeding
using a spoon did not exceed 30 minutes in 71% of the cases.

Table
3 presents the signs of risk for oral sensorimotor development. Greater
frequency of these signs was found among infants with gestational age of less
than or equal to 34 weeks than among those with gestational age of 35-36 weeks.
The sum of the risk factors resulted in an assessment index for the oral sensorimotor
system. Analysis of this index showed that the infants with gestational age
of less than 34 weeks presented a higher median for signs of risk for oral sensorimotor
development than did those with gestational age of 35-36 weeks (p=0.05).

Table
4 describes the results from the assessment of overall motor development
obtained using AIMS, in percentages. It was found that the percentage of infants
with AIMS score below the 10th percentile was significantly greater among those
with lower gestational age than among those with higher gestational age (p=0.009).

Table
5 shows that, among the infants with total AIMS score below the 25th percentile,
the median for the signs of risk for oral sensorimotor development was significantly
greater than among those with AIMS score between the 25th and 100th percentiles
(p<0.001).

Discussion

In this study, it was sought to assess oral sensorimotor
development and overall motor development in a sample of infants
with a history of prematurity, at a corrected chronological age
of four to five months.

Although the sample had few known risk factors for early
weaning, since these infants were recruited at a Baby Friendly
Hospital Initiative and their mothers were mostly adults and had
a reasonable level of schooling, it was found that a considerable
number of infants were not receiving exclusive breastfeeding at
the time of the assessment. This is contrary to the
recommendation from the Ministry of Health and the Pan-American
Health Organization (PAHO), which is that supplementary foods
should be offered from the sixth month of life onwards. The
habits of suckling on pacifiers, using bottle feeding and
increasing the flow by opening up the teat were also frequently
found in this population. As stated by Neiva et al. (2003),
Araújo (2004) and Vitolo (2003), these habits may have
contributed towards early weaning and possible alterations to the
evolution of the oral sensorimotor system.

In this population, it was seen in relation to supplementary
food that most of the infants accepted sweet foods of pasty
consistency (mashed fruits) that were offered on a spoon or
introduced into the infant's oral cavity on the mother's or a
caregiver's hand. The time spent on feeding most of the subjects
studied did not exceed 30 minutes. These findings show that the
infants presented good evolution regarding the grading of the
food consistency, which differs from the results from the studies
by Hawdon et al. (2000), Selley et al. (2001) and Monte and
Giugliani (2004), who found that their families had difficulty in
introducing supplementary food. However, the populations studied
by these authors consisted of preterm infants of very low
gestational age who presented pneumopathy and required prolonged
assisted mechanical ventilation. In our sample, there was lower
frequency and severity of perinatal complication, which explains
the difference in the results.

We also assessed signs of abnormalities relating to extra-oral
and intra-oral tactile sensitivity and found greater prevalence
of complaints when the tactile stimuli were deeper. Although it
was not possible to find any association between this and the
gestational age at birth and length of hospital stay, we can
infer that such behavior often occurred because of injuries that
occurred at the time of hospitalization and the family's lack of
capacity for promoting tactile and proprioceptive development
(Quresh et al., 2002; Als et al., 2004; Méio et al.,
2004).

The results found in the present study show that the children
born at younger gestational ages (<34 weeks) presented greater
numbers of signs of risk in the assessment index for the oral
sensorimotor system. These findings corroborate the data in the
literature, which suggest that there is a significant association
between the presence of signs of risk for oral sensorimotor
development and the gestational age at birth (Bly, 1994; Morris
and Klein, 2000; Hoekstra et al., 2004).

Also in this study, it was found that 26% of the infants
presented AIMS percentage score below the 10th percentile. The
most premature babies presented the lowest scores, thus
indicating retardation of overall motor development in relation
to weight support skills, postures adopted for motor tasks and
control over muscles working against gravity, at the corrected
chronological age of four to five months. Our results are
concordant with those of several authors, some of whom using AIMS
(Bartlett and Fanning, 2003) or other assessment techniques
(Gaetan and Ribeiro, 2002; Fallang et al., 2003). These authors
observed that preterm and full-term babies presented similar
postural control development up to the third month of life and
then started to present differences in their functional
repertoires.

Lekskulchai and Cole (2001) used a motor development
stimulation program on infants during their first three months of
life. They observed that the preterm newborns required
systematized multidisciplinary follow-up so that, at the
corrected chronological age of four months, they did not present
significant differences in motor performance, in comparison with
the same age group that had not been exposed to the risks
involved in prematurity. These authors suggested that
intervention programs might be effective in teaching the mothers
how to interact with and adequately stimulate their children,
thereby compensating for the biological risk of prematurity.

In the present study, the children who presented AIMS scores
below the 25th percentile had significantly higher medians for
the risk factors for oral sensorimotor development. This suggests
that there is an association between oral and overall motor
development, although the study design did not allow a causal
relationship to be established between them.

The beginning of modifications to infants' oral cavities, such
as the descent of the larynx (hyolaryngeal complex), is probably
associated with growth of the pharynx and the cervical column and
should be observed from the fourth month of life (Hiiemae et al.,
2002; Rogers and Arvedson, 2005).

Alexander et al. (1993) and also Bly (1994) concluded that the
muscles of the tongue and mandible (suprahyoid muscles) required
a support base for functional development. The cervical spine and
the scapular belt (junction with the infrahyoid muscles) are the
basis for this muscle control. Howle (2002) agreed with this
association, thus reinforcing the guidelines of the Bobath
neuroevolution concept, which states that the adaptive responses
needed for an individual's development are the result from
interactions between various systems, among which the overall
motor and oral sensorimotor systems.

It was seen in the present study that most of the infants did
not have extremely low gestational ages and were not affected by
severe morbidity. They were followed up by a speech therapist and
satisfactory performance was observed in relation to the
introduction of food orally at the age group assessed.

The humanized care
of the Kangaroo Mother Program that was provided for the infants in our sample
may also have contributed towards better self-regulation among the infants during
the neonatal period. It also favored a better mother-child relationship, which
probably reinforced the practice of stimulating the infants within their family
environments (Als et al. 2004; Andrade and Guedes, 2005).

Conclusion

In this study, larger numbers of abnormal signs were found in
assessing the development of the oral sensorimotor system of
infants with lower gestational age at birth, in comparison with
the group with greater gestational age. The abnormalities most
frequently found were the presence of primitive oral reflexes
(rooting, suckling and phasic bite), absence of lip contact,
absence of tongue activity in the frontal plane, absence of
symmetrical activity of the buccinator muscles, larynx in the
primitive elevated posture, absence of laryngeal elevation during
deglutition, absence of symmetrical arm activity in the medial
line, and also absence of gargling.

It was also observed that the most premature babies had lower
scores in the AIMS assessment, thus indicating risks for overall
motor development with regard to weight support skills, postures
adopted in motor tasks and control over muscles working against
gravity.

Although it was not possible to establish a causal
relationship between overall motor and oral sensorimotor
parameters, it can be inferred that the difficulties presented by
the infants regarding weight support skills, postures established
in motor tasks and control over muscles working against gravity
made it impossible to achieve developmental gains in the oral
sensorimotor system, because of the lack of stretching, symmetry
and synergy of the muscles that make up the trunk, scapular belt
and neck region.

These findings
show the need for follow-up by a speech therapy, using an approach based on
the interaction of the overall motor and oral sensorimotor parameters, since
these interact and contribute towards the development of motor processing for
language. These results further reinforce the need for more dynamic therapeutic
management that gives value to actions of multidisciplinary and transdisciplinary
nature, in which the various professionals involved will seek the best evidence
for appropriate follow-up and stimulation for infants with signs of risk for
neuropsychomotor development and oral sensorimotor development.

Acknowledgements

To the participating
families, to the staff of the "Professor Fernando Figueira" Mother and Child
Institute (IMIP) and to CNPq for the Research Productivity Grant for Professor
Marilia Lima.